Intestine-to-Germline Transmission of Epigenetic Information Intergenerationally Ensures Systemic Stress Resistance in C. elegans

Cell Rep. 2020 Mar 10;30(10):3207-3217.e4. doi: 10.1016/j.celrep.2020.02.050.

Abstract

Changes in epigenetic states affect organismal homeostasis, including stress resistance. However, the mechanisms coordinating epigenetic states and systemic stress resistance remain largely unknown. Here, we identify the intestine-to-germline communication of epigenetic states, which intergenerationally enhances stress resistance in C. elegans. The alterations in epigenetic states by deficiency of the histone H3K4me3 modifier ASH-2 in the intestine or germline increase organismal stress resistance, which is abrogated by knockdown of the H3K4 demethylase RBR-2. Remarkably, the increase in stress resistance induced by ASH-2 deficiency in the intestine is abrogated by RBR-2 knockdown in the germline, suggesting the intestine-to-germline transmission of epigenetic information. This communication from intestine to germline in the parental generation increases stress resistance in the next generation. Moreover, the intertissue communication is mediated partly by transcriptional regulation of F08F1.3. These results reveal that intertissue communication of epigenetic information provides mechanisms for intergenerational regulation of systemic stress resistance.

Keywords: ASH-2; Caenorhabditis elegans; DAF-16; RBR-2; epigenetics; germline; intergenerational inheritance; intertissue communication; intestine; oxidative stress resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / metabolism
  • Down-Regulation / genetics
  • Epigenesis, Genetic*
  • Germ Cells / metabolism*
  • Inheritance Patterns / genetics*
  • Intestines / physiology*
  • Oxidative Stress
  • Stress, Physiological / genetics*

Substances

  • Caenorhabditis elegans Proteins